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Diabetes Metab J 2013;37:140-148
http://dx.doi.org/10.4093/dmj.2013.37.2.140
pISSN 2233-6079 eISSN 2233-6087
Background: The purpose of this study was to evaluate the effects of high performance inulin supplementation on blood glycemic control and antioxidant status in women with type 2 diabetes.
Methods: In a randomized, triple-blind controlled trial, 49 females (fiber intake <30 g/day, 25<body mass index<35 kg/m2)
with type 2 diabetes were recruited from the Iran Diabetes Society and from endocrinology and metabolism clinics associated
with the Tabriz University of Medical Science. The participants were divided into one of two groups in which the participants either received 10 g/day of inulin (intervention, n=24) or maltodextrin (control, n=25) for 2 months. Fasting blood samples were
obtained and both glycemic control and antioxidant status were determined at baseline and at the end of the study.
Results: At the end of the study period, there were significant decreases in fasting plasma glucose (8.47%), glycosylated hemoglobin (10.43%), and malondialdehyde (37.21%) levels and significant increases in total antioxidant capacity (18.82%) and superoxide dismutase activity (4.36%) in the inulin group when compared to the maltodextrin group (P<0.05). Changes in fasting
insulin, homeostasis model assessment of insulin resistance, and catalase activity were not significant in the inulin group when
compared with the maltodextrin group. Glutathione peroxidase activity remained unchanged in both groups.
Conclusion: Inulin supplementation may improve some glycemic and antioxidant indices and decrease malondialdehyde levels
in women with type 2 diabetes. Further investigations are needed in order to confirm the positive effects that inulin may have on
the glycemic and antioxidant indices of patients with type 2 diabetes.
Keywords: Antioxidants; Diabetes mellitus, type 2; Insulin resistance; Inulin; Malondialdehyde
INTRODUCTION
Diabetes mellitus (DM) is a common health problem and is the
main cause of morbidity in developing and developed countries. The number of people with diabetes is gradually increasing, and its prevalence was reported to be 171 million people in
2000. It is estimated that at least 366 million people will suffer
from DM by the year 2030 [1]. In 2010, the prevalence of DM
was 8% and its health expenditure was equal to 600 million
Corresponding author: Parvin Dehghan
Student Research Center, Faculty of Health and Nutrition, Tabriz University
of Medical Sciences, Attar Nishaboori St., Golghasht St., Tabriz 51664, Iran
E-mail:dehghan.nut@gmail.com
Received: Sep. 19, 2012; Accepted: Jan. 3, 2013
U.S. dollars in the country of Iran [2]. DM is a metabolic disease that is characterized by the existence of hyperglycemia
along with having biochemical alterations of glucose, lipid profile, lipid peroxidation, insulin resistance and -cell dysfunction [3]. Prolonged exposure to hyperglycemia causes oxidative
stress and an imbalance of the oxidant/antioxidant status. Oxidative stress has been suggested to play a key role in the pathophysiology of type 2 diabetes and its complications [4].
Nowadays, functional foods are of interest due to their poThis is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/)
which permits unrestricted non-commercial use, distribution, and reproduction in any
medium, provided the original work is properly cited.
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tential health benefits [5]. The potential consequence of oxidative stress could be attenuated by the dietary consumption of
functional foods. Inulin-type fructans, a well-defined type of
functional foods, are naturally found in vegetables and fruits
such as: onions, garlic, chicory root, banana, and wheat, and
are used as prebiotic and dietary fiber in various food items.
Inulin-type fructans are indigestible carbohydrates, contain
fructose monomers that are linked by (12) bounds, and are
arranged as nonviscous, soluble, and fermentable fibers. High
performance (HP) inulin is a prebiotic that has a long-chain,
high-molecular weight mixes of inulin-type fructans, without
any fructans that have a degree of polymerization <10 [5].
This type of inulin is incorporated into baked goods, milk
products, drinks, and desserts as a substitute for sugar and/or
fat [6]. HP Inulin has a specific colonic fermentation property
that is able to change the composition of the gut microflora toward bifidobacteria. Ingestion of 5 to 8 g/day of inulin should
be sufficient to exhibit a positive effect on the gut microflora.
Possible side effects of inulin-type fructans can be seen at doses that are higher than 20 g/day [5].
The effects that inulin-type fructans have on reducing blood
glucose and oxidative stress has been shown in previous animal based studies [7,8]. To our knowledge, all of the human
studies to date have only assessed the effects of fructooligosaccharides (FOS), which have a lower molecular weight than HP
inulin, on diabetic patients and that there has been no study
that has yet assessed the effects of HP inulin on diabetic patients [9-11]. The results of the FOS studies on diabetic patients have been inconsistent. Yamashita et al. [9] has shown
that beneficial effects of oligofructose exist in regards to the
blood glucose and lipid profile of diabetic patients. In contrast,
a couple of other studies have failed to show any beneficial effects of inulin-type fructans in diabetic patients [10,11]. Due
to the probably beneficial effects of inulin-type fructans, especially on the carbohydrate metabolism [9, 12] and the antioxidant status [7,8], and the scarcity of data that exist on the
HP inulin effect on glycemic and antioxidant status, the present study was designed to assess the hypoglycemic and antioxidant effects of HP inulin in women with type 2 diabetes.
METHODS
Subjects
Sixty-five females with DM that were between the ages of 20
and 65 years of age had participated in the study. Participants
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were recruited from the Iranian Diabetic Society and from endocrinology and metabolism clinics that were associated with
the Tabriz University of Medical Science. Inclusion criteria
was defined as: having DM for more than 6 months, currently
having anti-diabetic treatment, having a stable diet and a body
mass index (BMI) >25 kg/m2 for the past 3 months. DM was
defined as having a fasting glucose level that is 126 mg/dL
[13]. Subjects were excluded if they had a history of gastrointestinal, pancreatic, or cardiovascular disease, renal, thyroid or
liver disturbance, being pregnant or lactating, consuming prebiotics, or probiotics, antibiotics, antacids, alcohol, antidiarrheal, anti-inflammatory or laxatives drugs, or lipid-lowering
medications 2 months prior to the intervention or during the
intervention, or if the individual had a typical fiber intake >30
g. Prior to the intervention, an appointment time was set for
each subjects to provide study information and to complete
their individual questionnaire and to provide their written informed consent. Demographic data including age, medication, and diabetes duration (in years) was obtained by using
the questionnaire. The study was approved by the Ethical
Committee of the Tabriz University of Medical Sciences and it
was registered on the Iranian Registry of Clinical Trials website (http://www.irct.ir/, IRCT201110293253N4).
Experimental design
The randomized control trial design was used to perform our
study in parallel and as a triple-blinded study. Both the participants and the researcher were blinded to the intervention.
Participants were randomly assigned in to one of two groups
by using a block randomization procedure, which matched
subjects to each block based on BMI and age. The experimental group received a daily supplement of 10 g of HP inulin
(Sensus, Roosendaal, The Netherlands) and the control group
received a similar amount of maltodextrin (Jiujiang Hurirong
Trade Co., Ltd, Jiujiang, China), which served as the placebo,
for 2 months. Daily supplements were divided in to two packages of 5 g each, which were instructed to be consumed with
breakfast and dinner along with a cup of water. The taste and
appearance of maltodextrin and inulin were similar to one another and the substrates were provided to the volunteers in
similar opaque packages. Subjects received half of their packages at the beginning of the study and received the remaining
packages in the middle of the study. In order to minimize the
dropout rate and to ensure the consumption of the supplements, the participants received a phone call once per week.
141
27 Inulin group
2 Medication change
1 Moved
24 Completed
142
27 Placebo group
25 Completed
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was adjusted between 0.5 to 0.6 absorbance units at 240 nm. The
reduction in the absorbance was measured. One unit of catalase
activity was defined as the amount of catalase that is fully absorbed in 30 seconds at 25C. The catalase activity was then calculated from the change in absorbance and was finally expressed
as units per milliliter [16].
Statistical analysis
Data were analyzed using the SPSS software version 17.0 (SPSS
Inc., Chicago, IL, USA). The results were expressed as mean
standard deviation. The normality of the distribution of data
was evaluated by the one-sample Kolmogorov-Smirnov test. For
quantitative variables, paired and unpaired sample t-tests were
used for means comparisons. The medications used in the two
groups were compared using the Mann-Whitney U test. Analysis of covariance (ANCOVA) was used to identify any differences between the two groups after intervention, and was adjusted for the baseline measurements and covariates. Differences
with a P<0.05 were considered to be statistically significant.
RESULTS
Variable
Period
Maltodextrin
(control)
group (n=25)
Inulin
group (n=24)
Initial
1,770.17205.60
1,693.60250.57
End
1,798.23238.95
1,417.86236.70a,b
Initial
224.7147.93
203.0064.31
End
223.3137.40
175.9250.34b
Initial
54.8511.86
51.2515.23
End
55.3314.70
54.2312.18
Initial
52.9113.34
54.3112.15
End
51.8314.91
45.628.70a,b
Initial
18.356.62
10.604.60c
End
14.923.95
12.954.30
Maltodextrin
(control)
group (n=25)
Inulin
group (n=24)
Energy, kcal
Age, yr
48.699.74
47.7710.14
Carbohydrate, g
Weight, kg
70.5311.05
75.4011.31
Characteristic
Height, cm
153.506.50
154.405.82
BMI, kg/m2
29.904.24
31.614.09
Diabetes duration, yr
5.334.60
7.335.42
2.710.94
2.851.08
1.961.17
2.290.99
Values are presented as meanstandard deviation. For all characteristics, there were no significant differences between the maltodextrin
and inulin groups (all P>0.05, based on independent samples t-tests).
BMI, body mass index.
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Protein, g
Total fat, g
Dietary fiber, g
143
regards to the glycemic indices and the oxidative stress parameters (Tables 3 and 4). At the end of the study, there was a significant decrease in the FPG (8.47%), HbA1c (10.43%), and
MDA (37.21%) in the inulin group when compared to that of
the maltodextrin group (P<0.05, ANCOVA when adjusted for
dietary fiber, energy changes, weight changes, and baselines
values). We observed no significant reduction in the fasting
insulin (34.32%) or the HOMA-IR (39.48%) in the inulin
group when compared to the maltodextrin group (P>0.05,
analysis of the covariance when adjusted for dietary fiber, energy changes, weight changes, and baselines values).
Inulin supplementation caused a 18.82% increase in the
TAC and a 4.36% increase in the SOD when compared with
the maltodextrin group after adjusting for dietary fiber, energy
changes, weight changes and baselines values (P<0.05). The
TAC levels increased (0.850.15 to 1.010.17 mmol/L) and
the MDA levels decreased (3.751.81 to 2.701.50 nmol/mL)
in the inulin group (P<0.05). Levels of catalase increased in
the inulin group (P<0.05, paired t-test), but this change was
not significant when compared to that of the maltodextrin
group (P>0.05, ANCOVA adjusted for dietary fiber, energy
changes, weight changes, and baseline values). GSH-Px activity remained unchanged in both groups. In the maltodextrin
group the TAC, MDA, SOD, and catalase changes that were
observed were not significant.
Table 3. Effects of 2 months of inulin or maltodextrin supplementation on glycemic indices in studied subjects
Variable
Period
Maltodextrin
(control)
group (n=25)
FPG, mg/dL
Initial
157.7610.60
161.6815.10
End
156.1214.17
146.6019.90
Initial
8.200.94
8.400.94
End
8.301.09
7.700.69a,b
HbA1c, %
HOMA-IR
Inulin
group (n=24)
a,b
13.163.80
14.034.30
End
13.444.80
9.293.20a
Initial
5.151.60
5.602.00
End
5.201.60
3.401.40
a
a
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DISCUSSION
High fiber diets can be beneficial in the prevention and management of diabetes. Some studies have reported that prebiotic
fibers may have a dominant effect on the control of diabetes
[17]. Therefore, in this clinical trial, we investigated the effect
that HP inulin supplementation has on glycemic indices and
on antioxidant markers of type 2 diabetic patients. Our results
showed that two months of HP inulin supplementation significantly decreased body weight and BMI when compared to the
group that received maltodextrin supplementation. Similar results have been shown with oligofructose supplementation in
animal studies and in studies with diabetic patients [11,18,19].
Parnell and Reimer [20] have reported that the supplementation of healthy adults with oligofructose at a dose of 21 g/day
for 12 weeks decreased body weight. In our study, the energy
intake of the inulin group significantly decreased (1,693.60
250.57 to 1,417.86236.70, P<0.05). The exact mechanism(s)
of weight reduction by inulin remains unclear. Some gut satiety hormones, especially those that are responsive to diet composition, including glucagon-like peptide 1 (GLP-1), PYY, and
ghrelin, are proposed to influence weight reduction [21].
In order to consider weight reduction as a main intervenTable 4. Effects of 2 months of inulin or maltodextrin supplementation on the antioxidative indices and MDA in studied
subjects
Variable
Period
Maltodextrin
(control)
group (n=25)
Inulin
group (n=24)
TAC, mmol/L
Initial
0.890.10
0.850.15
End
0.850.19
1.010.17a,b
SOD, U/mg Hb
GSH-Px, U/g Hb
Catalase, U/g Hb
MDA, nmol/mL
Initial
1,599.64138.15
1,566.18128.87
End
1,580.00144.55
1,648.97139.07a,b
Initial
33.402.62
33.202.42
End
33.312.80
33.702.60
Initial
66.5017.70
59.9217.40
End
65.0118.37
72.9526.02a
Initial
3.771.24
3.751.81
End
4.301.90
2.701.50a,b
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tional cause of observed changes in studied biochemical parameters, we included it in the ANCOVA model as a confounding factor. After the adjustment for weight reduction,
and energy intake, we showed that 2 months of inulin supplementation reduced the FPG, HbA1c, fasting insulin, and
HOMA-IR when compared to that of the maltodextrin group.
There were no statistically significant differences in the fasting
insulin and HOMA-IR between the two groups.
To the best of our knowledge there have not been any studies to date on the HP inulin effects in diabetic patients and
there have only been three studies that have investigated the
effects of fructans other than HP inulin on glucose and insulin
in type 2 DM patients [9-11]. Yamashita et al. [9] have shown
that oligofructose supplementation at a dose of 8 g/day for 2
weeks decreased the FPG levels in type 2 DM patients. Luo et
al. [10] and Alles et al. [11] have reported that there were no
significant changes that were observed with oligofructose supplementation, on FPG fasting insulin in patients with type 2
DM.
Jackson et al. [22] and Giacco et al. [23] have shown that
prebiotic supplementation (10 g/day inulin for 8 weeks in
healthy subjects and 10 g/day of short-chain-fructo-oligosaccharides for 2 months in individuals with mild hypercholesterolaemia, respectively) decreased fasting insulin. Russo et al.
[24] have reported that a significant decrease in HbA1c and
HOMA-IR in healthy young volunteers can be achieved by introducing inulin-enriched pasta. The different results obtained
in these studies may be explained by the dose and the kind of
supplementation, pathologic state and basal levels of the glycemic indices of the type 2 DM patients being studied.
Several mechanisms have been proposed to explain the hypoglycemic effect of fibers. Soluble fibers, such as inulin, can
control or lower serum glucose by delaying gastric emptying,
retarding entry of glucose into the blood stream, and reducing
the post-meal rise of serum glucose [25]. Also, the modification of the secretion of the gut hormones such as GLP-1 [26]
and short-chain fatty acids (SCFA), which are produced from
colonic fermentation of prebiotics [27], can affect serum glucose and insulin levels. SCFA may play a role in the so-called
ileocolonic brake, which explains the inhibition of gastric
emptying when nutrients reach the ileocolonic junction [27].
Oligofructose also increases glucose tolerance with increasing
levels of GLP-1, plasma insulin, pancreatic insulin, and -cell
mass [19], as well as an increase of GLP-2 [18].
Lipid peroxidation is higher in type 2 DM patients. Reduced
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145
146
ple size and a short intervention time. We did not measure serum fatty acids or take into consideration the glucose clamp.
We also did not define gut microflora changes with inulin supplementation. Measuring of other oxidative stress indices, such
as F2-isoprostanes, could strengthen the results of our study.
In conclusion, the results of this study showed that inulin
supplementation reduces body weight and improves glycemic
indices, antioxidant indices, and the MDA levels in type 2 DM
patients. These findings suggest a safe and inexpensive intervention for the management of type 2 DM. Further investigations are needed in order to confirm the positive effect that inulin had on the glycemic and antioxidant indices and the
MDA in type 2 DM patients.
CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.
ACKNOWLEDGMENTS
The authors would like to thank all of the patients for their
participation in this study. They would also like to thank Mr.
Firuz Purrahim for his help in recruiting these participants
and also to Mr. Amir M. Vatankhah for his technical assistance throughout this project. This research project was also
financially supported by the Health and Nutrition Faculty of
the Nutrition Research Center and the Vice Chancellor of Research of the Tabriz University of Medical Sciences in Iran.
This article was written based on the data from a PhD thesis
on nutrition, which was registered in the Tabriz University of
Medical Sciences.
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